New fossil insect order Permopsocida elucidates major radiation and evolution of suction feeding in hemimetabolous insects (Hexapoda: Acercaria).

Di-Ying Huang,Romain Garrouste,Dany Azar,Arnold H Staniczek,Alexey S Shmakov,Günter Bechly,Patricia Nel,Lars Krogmann,Rainer Ohlhoff,Tomy Dos Santos Rolo,André Nel,Michael S Engel,Thomas Van De Kamp,Chen-Yang Cai,Tilo Baumbach,Thierry Bourgoin,Jakub Prokop

doi:10.1038/srep23004

Abstract

With nearly 100,000 species, the Acercaria (lice, plant lices, thrips, bugs) including number of economically important species is one of the most successful insect lineages. However, its phylogeny and evolution of mouthparts among other issues remain debatable. Here new methods of preparation permitted the comprehensive anatomical description of insect inclusions from mid-Cretaceous Burmese amber in astonishing detail. These “missing links” fossils, attributed to a new order Permopsocida, provide crucial evidence for reconstructing the phylogenetic relationships in the Acercaria, supporting its monophyly, and questioning the position of Psocodea as sister group of holometabolans in the most recent phylogenomic study. Permopsocida resolves as sister group of Thripida + Hemiptera and represents an evolutionary link documenting the transition from chewing to piercing mouthparts in relation to suction feeding. Identification of gut contents as angiosperm pollen documents an ecological role of Permopsocida as early pollen feeders with relatively unspecialized mouthparts. This group existed for 185 million years, but has never been diverse and was superseded by new pollenivorous pollinators during the Cretaceous co-evolution of insects and flowers. The key innovation of suction feeding with piercing mouthparts is identified as main event that triggered the huge post-Carboniferous radiation of hemipterans, and facilitated the spreading of pathogenic vectors.

Highlights

The extraordinary diversity and success of insects is mainly based on two large radiations in Holometabola and Acercaria[1]
We propose a new phylogeny of Acercaria, based on morphological characters; some were obtained after the study of Psocorrhyncha
Our phylogenetic analysis confirms the monophyly of Acercaria including Psocodea (Fig. 3, Fig. S12), and questions the sister group relationship of the latter taxon with Holometabola that was recently proposed in the extensive phylogenomic analysis by the 1Kite project[2]

Summary

Introduction

The extraordinary diversity and success of insects is mainly based on two large radiations in Holometabola and Acercaria[1]. Increasing species diversity from barklice to thrips and bugs corresponds to the evolutionary transition from chewing mouthparts to stylet-like sucking-piercing mouthparts This major transformation represented one of the last remaining enigmas in the evolutionary history of insects, because the phylogeny of Acercaria was still unresolved[2,3,4,5]. We report and describe the new key taxon Psocorrhyncha burmitica, based on recently discovered fossils from mid-Cretaceous Burmite amber (Figs 1 and 2). They are related to less-completely known compression fossils, together representing the new order Permopsocida spanning the Permian-Cretaceous. Our Scanning Electron Microscopy (SEM) analysis of extracted pollen from the gut contents allowed a determination of angiosperms of the extant family Nyssaceae (tupelo trees) as host plants (Fig. 1)

Methods

Results

Conclusion